King, K.C. and McLaughlin, J. Daniel and Gendron, A.D. and Pauli, B.D. and Giroux, I. and Rondeau, B. and Boily, M. and Juneau, P. and Marcogliese, D.J. (2007) Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology, 134 (14). pp. 2063-2080. ISSN 0031-1820
- Published Version
Official URL: http://dx.doi.org/10.1017/S0031182007003277
Given that numerous amphibians are suffering population declines, it is becoming increasingly important to examine the relationship between disease and environmental disturbance. Indeed, while many studies relate anthropogenic activity to changes in the parasitism of snails and fishes, little is known of the impact on the parasites of amphibians, particularly from agriculture. For 2 years, the parasite communities of metamorphic northern leopard frogs from 7 agricultural wetlands were compared with those from 2 reference wetlands to study differences in parasite community diversity and abundance of various species under pristine conditions and 3 categories of disturbance: only agricultural landscape, only pesticides, and agricultural landscape with pesticides. Agricultural (and urban) area was negatively related to species richness, and associated with the near absence of adult parasites and species that infect birds or mammals. We suggest that agriculture and urbanization may hinder parasite transmission to frogs by limiting access of other vertebrate hosts of their parasites to wetlands. The only parasite found at all localities was an unidentified echinostome infecting the kidneys. This parasite dominated communities in localities surrounded by the most agricultural land, suggesting generalist parasites may persist in disrupted habitats. Community composition was associated with dissolved organic carbon and conductivity, but few links were found with pesticides. Pollution effects may be masked by a strong impact of land use on parasite transmission.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||King, K.C. and McLaughlin, J. Daniel and Gendron, A.D. and Pauli, B.D. and Giroux, I. and Rondeau, B. and Boily, M. and Juneau, P. and Marcogliese, D.J.|
|Journal or Publication:||Parasitology|
|Digital Object Identifier (DOI):||10.1017/S0031182007003277|
|Keywords:||parasite communities; amphibians; species richness; Rana pipiens; agriculture; pesticides; land use; urbanization; wetlands|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||13 Jul 2010 16:04|
|Last Modified:||24 Aug 2016 21:26|
Amezaga, J. M., Santamaría, L. and Green, A. J. (2002). Biotic wetland connectivity – supporting a new approach for wetland policy. Acta Oecologica 23, 213–222.
Beasley, V. R., Faeh, S. A., Wikoff, B., Staehle, C., Eisold, J., Nichols, D., Cole, R., Schotthoefer, A. M., Greenwell, M. and Brown, L. E. (2005). Risk factors and declines in northern cricket frogs (Acris crepitans). In Declining Amphibians: a United States Response to the Global Phenomenon (ed. Lannoo, M. J.), pp. 75–86. University of California Press, Berkeley, USA.
Beaven, L., Sadler, J. and Pinder, C. (2001). The invertebrate fauna of a physically modified urban river. Hydrobiologia 445, 97–108.
Bradley, C. A. and Altizer, S. (2006). Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95–102.
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.
Canadian Council of Ministers of the Environment. (2001). Canadian Water Quality Guidelines (CWQG) for the Protection of Aquatic Life. Environment Canada, Ottawa.
Carey, C., Bradford, D. F., Brunner, J. L., Collins, J. P., Davidson, E. W., Longcore, J. E., Ouellet, M., Pessier, A. P. and Schock, D. M. (2003). Biotic factors in amphibian population declines. In Amphibian Decline: An Integrated Analysis of Multiple Stressor Effects (ed. Linder, G. L., Krest, S. and Sparling, D.), pp. 153–208. Society of Environmental Toxicology and Chemistry (SETAC), Pensacola, FL, USA.
Carey, C. and Bryant, C. J. (1995). Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environmental Health Perspectives 103 (Suppl.), S13–S17.
Carpenter, S. R., Caraco, N. F., Correll, D. L., Howarth, R. W., Sharpley, A. N. and Smith, V. H. (1998). Non-point pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8, 559–568.
Carrier, S. (2001). National Laboratory for Environmental Testing, 2001–02 Sample Collection Summary. Environment Canada, National Water Research Institute, Burlington/Saskatoon.
Christin, M. S., Gendron, A. D., Brousseau, P., Menard, L., Marcogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22, 1127–1133.
Christin, M. S., Ménard, L., Gendron, A. D., Ruby, S., Cyr, D., Marcogliese, D. J., Rollins-Smith, L. and Fournier, M. (2004). Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquatic Toxicology 67, 33–43.
Clarke, A. H. (1981). The Freshwater Molluscs of Canada. National Museums of Canada, Ottawa.
Cone, D. K., Marcogliese, D. J. and Watt, W. D. (1993). Metazoan parasite communities of yellow eels (Anguilla rostrata) in acidic and limed rivers of Nova Scotia. Canadian Journal of Zoology 71, 177–184.
Conover, W. J. and Iman, R. L. (1981). Rank transformations as a bridge between parametric and nonparametric statistics. American Statistician 35, 124–136.
Czech, H. A. and Parsons, K. C. (2002). Agricultural wetlands and waterbirds: a review. Waterbirds 25 (Special Publication 2), 25–41.
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2003). Infectious disease and amphibian population declines. Diversity and Distributions 9, 141–150.
Davies, P. E. and Nelson, M. (1994). Relationships between riparian buffer widths and the effects of logging on stream habitat, invertebrate community composition and fish abundance. Australian Journal of Marine and Freshwater Research 45, 1289–1305.
Desroches, J. F. and Rodrigue, D. (2004). Amphibiens et reptiles du Québec et des maritimes. Éditions Michel Quintin, Waterloo.
Gendron, A. D., Marcogliese, D. J., Barbeau, S., Christin, M. S., Brousseau, P., Ruby, S., Cyr, D. and Fournier, M. (2003). Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135, 469–476.
Gibbs, J. P. (2000). Wetland loss and biodiversity conservation. Conservation Biology 14, 314–317.
Gilbertson, M. K., Haffner, G. D., Drouillard, K. G., Albert, A. and Dixon, B. (2003). Immunosuppression in the northern leopard frog (Rana pipiens) induced by pesticide exposure. Environmental Toxicology and Chemistry 22, 101–110.
Gillilland, M. G. III and Muzzall, P. M. (1999). Helminths infecting froglets of the northern leopard frog (Rana pipiens) from Foggy Bottom Marsh, Michigan. Journal of the Helminthological Society of Washington 66, 73–77.
Giroux, I. (1999). Contamination de l'eau par les Pesticides dans les Régions de Culture de Maïs et de Soya au Québec. Direction des écosystèmes aquatiques, Ministère de l'Environnement, Quebec.
Giroux, I. (2002). Contamination de l'eau par les Pesticides dans les Régions de Culture de Maïs et de Soya au Québec. Direction des écosystèmes aquatiques, Ministère de l'Environnement, Quebec.
Goater, T. M. and Goater, C. P. (2001). Ecological monitoring and assessment network: Protocols for measuring biodiversity: Parasites of amphibians and reptiles. http://www.eman-rese.ca/eman/ecotools/protocols/terrestrial/herp_parasites/intro.html
Green, D. M. (2005). The biology of amphibian declines. In Declining Amphibians: a United States Response to the Global Phenomenon (ed. Lannoo, M. J.), pp. 58–72. University of California Press, Berkeley, USA.
Hamann, M. I., Kehr, A. I. and González, C. E. (2006). Species affinity and infracommunity ordination of helminths of Leptodactylus chaqensis (Anura: Letpdactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92, 1171–1179.
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 1059–1066.
Hernandez, A. D., Bunnel, J. F. and Sukhdeo, M. V. K. (2007). Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems. Parasitology 134, 91–102.
Heyer, R. A., Donnelly, M. A., McDiarmid, R. W., Hayek, L.-A. C. and Foster, M. S. (1994). Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington.
Houlahan, J. E. and Findlay, C. S. (2003). The effects of adjacent land use on wetland amphibian species richness and community composition. Canadian Journal of Fisheries and Aquatic Sciences 60, 1078–1094.
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 7, 381–385.
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.
Huspeni, T. C. and Lafferty, K. D. (2004). Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 14, 795–804.
Johnson, P. T. J. and Chase, J. M. (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521–526.
Jones, J. J., Lortie, J. P. and Pierce, U. D. (1988). The Identification and Management of Significant Fish and Wildlife Resources in Southern Coastal Maine. Maine Department of Inland Fisheries and Wildlife, Augusta,, USA.
Jones, E. B. D., Helfman, G. S., Harper, J. O. and Bolstad, P. V. (1999). Effects of riparian forest removal on fish assemblages in southern Appalachian streams. Conservation Biology 13, 1454–1465.
Keas, B. and Blankespoor, H. D. (1997). The prevalence of cercariae from Stagnicola emarginata over 50 years in Northern Michigan. Journal of Parasitology 83, 536–540.
Kennedy, C. R. (1997). Freshwater fish parasites and environmental quality: an overview and caution. Parassitologia 39, 249–254.
Khan, R. A. and Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201–238.
Kiesecker, J. M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences, USA 99, 9900–9904.
Kiesecker, J. M., Belden, L. K., Katriona, S. and Rubbo, M. J. (2004). Amphibian decline and emerging disease: What can sick frogs teach us about new and resurgent diseases in human populations and other species of wildlife? American Scientist 92, 139–147.
Kiesecker, J. M., Blaustein, A. R. and Belden, L. K. (2001). Complex causes of amphibian population declines. Nature, London 410, 681–684.
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006a). Environmental factors influencing trematode prevalence in the grey tree frog (Hyla versicolor) tadpoles in southern Ontario. Journal of Parasitology 92, 997–1001.
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006b). Effects of atrazine on cercarial longevity, activity, and infectivity. Journal of Parasitology 92, 306–311.
Kostadinova, A. and Gibson, D. I. (2000). The systematics of the echinostomes. In Echinostomes as Experimental Models for Biological Research (ed. Fried, B. and Graczyk, T. K.), pp. 31–57. Kluwer, Dordrecht, The Netherlands.
Kuris, A. M. and Lafferty, K. D. (1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189–217.
Laboratoire du Centre Saint-Laurent. (1994). Manuel des Méthodes d'Analyse: Partie 1 (Analyses Physico-Chimiques). Partie 2 (Analyse des Paramètres Inorganiques). Environnement Canada, Conservation de l'environnement, Centre Saint-Laurent, Montreal.
Lafferty, K. D. (1997). Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.
Lafferty, K. D. and Holt, R. D. (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654–664.
Lafferty, K. D. and Kuris, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925–931.
Lafferty, K. D. and Kuris, A. M. (2005). Parasitism and environmental disturbances. In Parasitism and Ecosystems (ed. Thomas, F, Guégan, J. F. and Renaud, F.), pp. 113–123. Oxford University Press, London.
Laurila, A., Pakkasmaa, S., Crochet, P. A. and Merilä, J. (2002). Predator-induced plasticity in early life-history and morphology in two anuran amphibians. Oecologia 132, 524–530.
Laurila, A., Pakkasmaa, S. and Merilä, J. (2001). Influence of seasonal time constraints on growth and development of common frog tadpoles: a photoperiod experiment. Oikos 95, 451–460.
Leclair, R. and Castanet, J. (1987). Skeletochronological assessment of age and growth in the frog Rana pipiens Schreber (Amphibia, Anura) from Southwestern Quebec. Copeia 2, 361–369. OpenURL CrossRef Google Scholar
Legendre, P. and Legendre, L. (1998). Numerical Ecology, 2nd Edn. Elsevier, Oxford.
Lemieux, C., Quémerais, B. and Lum, K. R. (1995). Seasonal patterns of atrazine loading for the St. Lawrence River (Canada) and its tributaries. Water Research 29, 1491–1504.
Loman, J. and Lardner, B. (2006). Does pond quality limit frogs Rana arvalis and Rana temporaria in agricultural landscapes? A field experiment. Journal of Applied Ecology 43, 690–700.
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–114.
MacKenzie, K. (1999). Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38, 955–959.
Magurran, A. E. (1988). Ecological Diversity and Its Measurement. Princeton University Press, Princeton, USA.
Marcogliese, D. J. (2003). Food webs and biodiversity: are parasites the missing link? Journal of Parasitology (Suppl.) 89, S106–S113. OpenURL Google Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. Ecohealth 1, 151–164.
Marcogliese, D. J. (2005). Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705–716.
Marcogliese, D. J., Ball, M. and Lankester, M. W. (2001). Potential impacts of clearcutting on parasites of minnows in small boreal lakes. Folia Parasitologica 48, 269–274.
Marcogliese, D. J. and Cone, D. K. (1997). Parasite communities as indicators of ecosystem stress. Parassitologia 39, 227–232.
Marcogliese, D. J., Gagnon Brambilla, L., Gagné, F. and Gendron, A. D. (2005). Joint effects of parasitism and pollution on biomarkers of oxidative stress in yellow perch (Perca flavescens). Diseases of Aquatic Organisms 63, 77–84.
Marcogliese, D. J., Gendron, A. D., Plante, C., Fournier, M. and Cyr, D. (2006). Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: effects of municipal effluents and habitat. Canadian Journal of Zoology 84, 1461–1481.
Matson, P. A., Parton, W. J., Power, A. G. and Swift, M. J. (1997). Agricultural intensification and ecosystem properties. Science 277, 504–509.
McAlpine, D. F. and Burt, M. D. B. (1998). Helminths of bullfrogs (Rana catesbeiana), green frogs (Rana clamitans), and leopard frogs (Rana pipiens) in New Brunswick. Canadian Field-Naturalist 112, 50–68.
McDonald, M. E. (1969). Annotated Bibliography of Helminths of Waterfowl (Anatidae). Bureau of Sport Fisheries and Wildlife Special Scientific Report No. 125, Washington.
McKenzie, V. J. (2007). Human land use and patterns of parasitism in tropical amphibian hosts. Biological Conservation 137, 102–116.
McMahon, R. F. and Bogan, A. E. (2001). Mollusca: Bivalvia. In Ecology and Classification of North American Freshwater Invertebrates, 2nd Edn (ed. Thorp, J. H. and Covich, A. P.), pp. 297–325. Academic Press, San Diego, USA.
Moore, A. A. and Palmer, M. A. (2005). Invertebrate biodiversity in agricultural and urban headwater streams: implications for conservation and management. Ecological Applications 15, 1169–1177.
Muzzall, P. M. (2005). Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature 1916–2003. Fisheries Research Report No. 2077. State of Michigan Department of Natural Resources, Ann Arbor, USA.
Environment Canada. (2005). A Literature Review of Risks and Benefits of Agriculture to Biodiversity and Biodiversity to Agriculture. National Agri-Environmental Standards Initiative Technical Series Report 1–15, Gatineau,, Canada.
Olsen, O. W. (1974). Animal Parasites: Their Life Cycles and Ecology, 3rd Edn. University Park Press, Baltimore, USA.
Overstreet, R. M. and Howse, H. D. (1977). Some parasites and diseases of estuarine fishes in polluted habitats of Mississippi. Annals of the New York Academy of Sciences 298, 437–462.
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–298.
Poulin, R. (1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 58–61.
Prudhoe, S. and Bray, R. A. (1982). Platyhelminth Parasites of the Amphibia. Oxford University Press, London.
Rau, M. E., Doyle, J. and Gordon, D. (1978). Les parasites des animaux sauvages du Québec. 2. Les parasites des grenouilles et des serpents de la région de l'Île Perrot. Le Naturaliste Canadien 105, 56–57.
Relyea, R. A. (2004). Growth and survival of five amphibian species exposed to combinations of pesticides. Environmental Toxicology and Chemistry 23, 1737–1742.
Schotthoefer, A. M., Cole, R. A. and Beasley, V. R. (2003). Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89, 475–482.
Scott, D. E. (1990). Effect of larval density of Ambystoma opacum: an experiment in large-scale field enclosures. Ecology 71, 296–306.
Seburn, C. N. L. and Seburn, D. C. (1998). Status Report: Northern Leopard Frog Rana pipiens (Western Populatio
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